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Shell Clamping Behaviour in a Limpet 541 The Journal of Experimental Biology 205, 539–547 (2002) 539 Printed in Great Britain © The Company of Biologists Limited 2002 JEB3898 Shell clamping behaviour in the limpet Cellana tramoserica Gary K. Ellem1,*, John E. Furst2 and Kenneth D. Zimmerman2 1Department of Biological Sciences, University of Newcastle, Callaghan, NSW 2308, Australia and 2School of Science and Technology, Central Coast Campus, University of Newcastle, Brush Road, Ourimbah, NSW 2258, Australia *e-mail: [email protected] Accepted 5 December 2001 Summary The behaviour of clamping the shell against the predator attack, limpets clamped tightly for several substratum may play an important role in the limpet minutes. In response to lifting forces applied to the shell, adhesion mechanism because friction generated by this limpets clamped at a set proportion of the lifting force, behaviour resists dislodgement by shear forces. This paper even if the lift force was a highly dynamic wave profile. describes the development of an apparatus to analyse This behaviour has implications for numerical models that limpet clamping activity in relation to known forces, attempt to describe limpet adhesion because it shows that including simulated wave activity and predator attack. limpets cannot be represented by a simple mechanical The results show that Cellana tramoserica clamps its shell analogue and that the clamping behaviour must be in a closely regulated manner consistent with an active accounted for if useful predictions are to be drawn. role in the limpet adhesion mechanism. Limpets clamped sharply for several seconds in response to single disturbances such as tapping the shell. In response to Key words: limpet, Cellana tramoserica, shell clamping, behaviour, more continuous disturbance simulating a concerted adhesion, defence, force, wave action. Introduction It is widely acknowledged that limpets ‘clamp’ or ‘hunker suction provides good resistance to hydrodynamic lift, it down’ when disturbed in an effort to prevent dislodgement provides poor resistance to shear forces. In this paper, we (Cook et al., 1969; McAlister and Fisher, 1968). Until now, propose that limpets clamp their shell against the substratum however, there has been no attempt to quantify the clamping to generate a frictional force that resists horizontal shear. Shell response or to investigate its role in the limpet adherence clamping against the substratum uses the vertical adherence mechanism. This lack of information regarding clamping has strength of the suction mechanism to create a frictional force meant that models of limpet adhesion/shell shape have been that resists the shear force of hydrodynamic drag. Fig. 1 unable to include clamping and, hence, treat limpets as outlines the forces exerted on the limpet while exposed to fluid mechanical structures rather than biological organisms that flow. may be able to respond to applied forces (Denny, 2000). This Smith (1991b) showed that the force with which limpets arguably limits the accuracy of these models, particularly their adhere to the substratum is often greater than the force applied ability to provide insight into the selection of limpet structural to the shell during detachment. Although this result may have characteristics and the metabolic costs of adhesion (Santini et been indicative of shell clamping behaviour, the apparatus used al., 1995). by Smith (1991b) (which was designed to investigate the role Shell clamping brings the lower rim of the conical shell of of suction in the adherence of limpets) was not able to isolate a limpet into direct contact with the substratum. This creates clamping from other mechanisms that may lower the pressure friction between the shell and substratum that provides beneath the foot. A complete analysis of clamping behaviour increased resistance to horizontal shear and prevents requires an ability to differentiate between these mechanisms dislodgement. Most studies that observed clamping involved so that the role of each in adhesion may be understood. the role of clamping as a defence against predators (Branch and The ideal experiment to verify the use of clamping by Cherry, 1985; Thompson et al., 2000), although Denny (1988) limpets in resisting drag would be to measure the forces of lift suggested that clamping has a role in resisting hydrodynamic and drag induced by wave action on a number of limpets while drag. simultaneously measuring the force of shell clamping for the Smith (1992) found that limpets use suction while foraging same limpets. Thus, in an ideal experiment, the force of at high tide. This is a problem for limpets because, although clamping could be directly related to hydrodynamic forces, and 540 G. K. Ellem, J. E. Furst and K. D. Zimmerman Water velocity responses to wave action suggests that energy efficiency, not resistance to maximum wave forces, may be the primary selective force for limpet shell design. Lift Limpet Materials and methods Friction Drag The method developed for the measurement of shell clamping involved removing limpets from their natural Substratum environment and performing measurements in a laboratory Clamping Clamping under controlled conditions. While this technique had the force force obvious disadvantage of placing the limpets in a foreign Adherence environment that may have confounded their behaviour, it had the essential advantage that accurate measurements could be Fig. 1. A force diagram describing the forces acting during wave performed. Accurate measurement was required because the action. The model assumes that the limpet clamps its shell against the substratum in order to generate friction to resist horizontal shear. results showed that the clamping force was often an order of magnitude lower than the adherence force, and therefore difficult to detect in the absence of accurate measurements. the behavioural mechanics of limpet shell clamping would be known. Limpet collection and maintenance Unfortunately, both these tasks are difficult. It is impossible Cellana tramoserica (Holten 1802) longer than 27 mm were to measure directly the hydrodynamic forces that are placed on collected from exposed, sandstone platforms near Terrigal the limpet without resorting to placing the limpet on some (NSW, Australia). Limpets were removed from the substratum sort of force plate. Another technique may be to predict by placing the flattened tip of a diving knife under the leading hydrodynamic forces on the basis of flow measurements and edge of the shell and twisting the knife slowly. The majority shell shape parameters; however, the highly turbulent flow of of limpets collected in this way showed no sign of injury; the intertidal zone limits the precision with which the actual however, less than 5 % of the limpets, mainly those collected forces may be measured, and the magnitude of these errors is while exposed at low tide, showed signs of damage to the likely to dominate any evidence of behavioural regulation. It underside of the foot or musculature. It is thought that these is also difficult to measure the degree of shell clamping without limpets were using a glue-type adherence mechanism, as inserting something under the shell and, in doing so, changing described Smith (1992), and thus suffered greater injury the flow characteristics of the organism. It is not, therefore, because of their high adherence. Damaged limpets were feasible to measure either the hydrodynamic forces placed on discarded at the collection site. the organism in vivo or the behavioural response of the limpets The limpets were placed in a bucket of freshly collected sea to these forces in vivo. water. The bucket was lined with a netting bag to prevent the We decided to construct an apparatus that removed the limpets adhering to the side of the container. They were then vagaries of force measurement inherent in trying to conduct transported to a constant-temperature laboratory (18 °C), experiments in vivo. The apparatus was able to apply lifting where an air hose was inserted into the water to ensure forces to the limpet shell that could be accurately controlled oxygenation. Limpets remained in the bucket and were used and measured, allowing simulation of wave impact or other within 12 h of collection. force profiles, as required. The apparatus was also able to measure the force of shell clamping directly and independently Development of the apparatus of the pressure beneath the limpet foot and therefore could, We developed an apparatus that was able to measure directly unlike the apparatus of Smith (1991b), specifically identify and the forces acting during adhesion. Newton’s first law states quantify clamping for the first time. that, if the limpet remains adhered to the apparatus and does While a number of previous researchers have developed not undergo acceleration, then the sum of the force acting in apparatus to measure the adherence of intertidal organisms each direction must be zero. Hence, for forces acting in the (Branch and Marsh, 1978; Denny, 2000; Grenon and Walker, vertical direction during adhesion: 1981; Miller, 1974; Smith, 1991b; Thomas, 1948), none has attempted to measure limpet clamping responses or, with the FAdherence = FClamping + FLift , (1) exception of Smith (Smith, 1991b), addressed behavioural where FAdherence is the tensile force placed by the foot on the responses. The results presented here suggest that shell substratum, FClamping is the force with which the covering shell clamping behaviour is an active component of the limpet is clamped against the substratum and FLift is the simulated lift adherence mechanism of resistance to wave action. This has force applied by the apparatus to the limpet shell. FAdherence is implications not only for biomechanical models of adhesion not to be confused with the maximum force of adhesion, or but also in identifying the pressures of natural selection on FAdherence at adhesive failure, used in previous studies. shell design. Recognition that limpets have biologically active The apparatus was designed so that it could accurately Shell clamping behaviour in a limpet 541 Computer- substratum required the construction of a force cell that controlled isolated the tensile attachment of the foot.
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